Quantifying inbreeding avoidance through extra-pair reproduction.
Ontology highlight
ABSTRACT:
SUBMITTER: Reid JM
PROVIDER: S-EPMC4312944 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:One hypothesis explaining extra-pair reproduction is that socially monogamous females mate with extra-pair males to adjust the coefficient of inbreeding (f) of extra-pair offspring (EPO) relative to that of within-pair offspring (WPO) they would produce with their socially paired male. Such adjustment of offspring f requires non-random extra-pair reproduction with respect to relatedness, which is in turn often assumed to require some mechanism of explicit pre-copulatory or post-copulatory kin discrimination. We propose three demographic processes that could potentially cause mean f to differ between individual females' EPO and WPO given random extra-pair reproduction with available males without necessarily requiring explicit kin discrimination. Specifically, such a difference could arise if social pairings formed non-randomly with respect to relatedness or persisted non-randomly with respect to relatedness, or if the distribution of relatedness between females and their sets of potential mates changed during the period through which social pairings persisted. We used comprehensive pedigree and pairing data from free-living song sparrows (Melospiza melodia) to quantify these three processes and hence investigate how individual females could adjust mean offspring f through instantaneously random extra-pair reproduction. Female song sparrows tended to form social pairings with unrelated or distantly related males slightly less frequently than expected given random pairing within the defined set of available males. Furthermore, social pairings between more closely related mates tended to be more likely to persist across years than social pairings between less closely related mates. However, these effects were small and the mean relatedness between females and their sets of potential extra-pair males did not change substantially across the years through which social pairings persisted. Our framework and analyses illustrate how demographic and social structuring within populations might allow females to adjust mean f of offspring through random extra-pair reproduction without necessarily requiring explicit kin discrimination, implying that adjustment of offspring f might be an inevitable consequence of extra-pair reproduction. New theoretical and empirical studies are required to explore the general magnitude of such effects and quantify the degree to which they could facilitate or constrain long-term evolution of extra-pair reproduction.
| S-EPMC4670719 | biostudies-literature
Project description:Female extra-pair reproduction in socially monogamous systems is predicted to cause cuckolded socially-paired males to conditionally reduce paternal care, causing selection against extra-pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially-paired female and/or to her extra-pair mate, and therefore be related to extra-pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra-pair reproduction, might then be weakened. We derive metrics that quantify allele-sharing between within-pair and extra-pair offspring and their mother and her socially-paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra-pair reproduction and inbreeding on a brood's total allelic value to its socially-paired parents. Cuckolded male song sparrows were almost always detectably related to extra-pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra-pair reproduction, this decrease was reduced by within-pair and extra-pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra-pair reproduction, parental care, and inbreeding.
| S-EPMC4949684 | biostudies-literature
Project description:One key hypothesis explaining the evolution and persistence of polyandry, and resulting female extra-pair reproduction in socially monogamous systems, is that female propensity for extra-pair reproduction is positively genetically correlated with male reproductive fitness and consequently experiences positive cross-sex indirect selection. However, key genetic correlations have rarely been estimated, especially in free-living populations experiencing natural (co)variation in reproductive strategies and fitness. We used long-term life-history and pedigree data from song sparrows (Melospiza melodia) to estimate the cross-sex genetic correlation between female propensity for extra-pair reproduction and adult male lifetime reproductive success, and thereby test a key hypothesis regarding mating system evolution. There was substantial additive genetic variance in both traits, providing substantial potential for indirect selection on female reproductive strategy. However, the cross-sex genetic correlation was estimated to be close to zero. Such small correlations might arise because male reproductive success achieved through extra-pair paternity was strongly positively genetically correlated with success achieved through within-pair paternity, implying that the same successful males commonly sire offspring produced by polyandrous and monogamous females. Cross-sex indirect selection may consequently have limited capacity to drive evolution of female extra-pair reproduction, or hence underlying polyandry, in systems where multiple routes to paternity success exist.
| S-EPMC6121835 | biostudies-other
Project description:Avoiding inbreeding, and therefore avoiding inbreeding depression in offspring fitness, is widely assumed to be adaptive in systems with biparental reproduction. However, inbreeding can also confer an inclusive fitness benefit stemming from increased relatedness between parents and inbred offspring. Whether or not inbreeding or avoiding inbreeding is adaptive therefore depends on a balance between inbreeding depression and increased parent-offspring relatedness. Existing models of biparental inbreeding predict threshold values of inbreeding depression above which males and females should avoid inbreeding, and predict sexual conflict over inbreeding because these thresholds diverge. However, these models implicitly assume that if a focal individual avoids inbreeding, then both it and its rejected relative will subsequently outbreed. We show that relaxing this assumption of reciprocal outbreeding, and the assumption that focal individuals are themselves outbred, can substantially alter the predicted thresholds for inbreeding avoidance for focal males. Specifically, the magnitude of inbreeding depression below which inbreeding increases a focal male's inclusive fitness increases with increasing depression in the offspring of a focal female and her alternative mate, and it decreases with increasing relatedness between a focal male and a focal female's alternative mate, thereby altering the predicted zone of sexual conflict. Furthermore, a focal male's inclusive fitness gain from avoiding inbreeding is reduced by indirect opportunity costs if his rejected relative breeds with another relative of his. By demonstrating that variation in relatedness and inbreeding can affect intra- and inter-sexual conflict over inbreeding, our models lead to novel predictions for family dynamics. Specifically, parent-offspring conflict over inbreeding might depend on the alternative mates of rejected relatives, and male-male competition over inbreeding might lead to mixed inbreeding strategies. Making testable quantitative predictions regarding inbreeding strategies occurring in nature will therefore require new models that explicitly capture variation in relatedness and inbreeding among interacting population members.
| S-EPMC4409402 | biostudies-literature
Project description:Although most Hymenoptera reproduce via arrhenotokous haplodiploidy, the underlying genetic mechanisms vary. Of these, the most widespread mechanism appears to be single-locus complementary sex determination (sl-CSD), in which individuals that are diploid and heterozygous at a sex-determining locus are female, and individuals that are homozygous or hemizygous are male. Because inbreeding increases the probability of producing diploid males, which are often sterile or inviable, sl-CSD can generate substantial inbreeding depression. To counteract this, Hymenoptera with traits that promote inbreeding, such as gregariousness, may evolve one or more of the following: inbreeding avoidance, functional diploid males or alternative sex determination mechanisms. Here, we investigate sex determination, inbreeding depression and inbreeding avoidance in Neodiprion lecontei, a gregarious, pine-feeding sawfly in the family Diprionidae. First, via inbreeding experiments and flow cytometry, we demonstrate that this species has CSD. By modeling expected sex ratios under different conditions, we also show that our data are consistent with sl-CSD. Second, via tracking survival in inbred and outbred families, we demonstrate that inbred families have reduced larval survival and that this mortality is partly attributable to the death of diploid males. Third, using a no-choice mating assay, we demonstrate that females are less willing to mate with siblings than nonsiblings. Together, these results suggest that inbreeding depression stemming from CSD has shaped mating behavior in N. lecontei. These results also set the stage for future comparative work that will investigate the interplay between sex determination, ecology and behavior in additional diprionid species that vary in larval gregariousness.
| S-EPMC5061915 | biostudies-literature
Project description:Mechanisms reducing inbreeding are thought to have evolved owing to fitness costs of breeding with close relatives. In small and isolated populations, or populations with skewed age- or sex distributions, mate choice becomes limited, and inbreeding avoidance mechanisms ineffective. We used a unique individual-based dataset on moose from a small island in Norway to assess whether inbreeding avoidance was related to population structure and size, expecting inbreeding avoidance to be greater in years with larger populations and even adult sex ratios. The probability that a potential mating event was realized was negatively related to the inbreeding coefficient of the potential offspring, with a stronger relationship in years with a higher proportion or number of males in the population. Thus, adult sex ratio and population size affect the degree of inbreeding avoidance. Consequently, conservation managers should aim for sex ratios that facilitate inbreeding avoidance, especially in small and isolated populations.
| S-EPMC4298189 | biostudies-literature
Project description:The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (cov(A)) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate cov(A) between a female's liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of cov(A) were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.
| S-EPMC3479734 | biostudies-literature
Project description:Extra-pair paternity is the result of copulation between a female and a male other than her social partner. In socially monogamous birds, old males are most likely to sire extra-pair offspring. The male manipulation and female choice hypotheses predict that age-specific male mating behaviour could explain this old-over-young male advantage. These hypotheses have been difficult to test because copulations and the individuals involved are hard to observe. Here, we studied the mating behaviour and pairing contexts of captive house sparrows, Passer domesticus. Our set-up mimicked the complex social environment experienced by wild house sparrows. We found that middle-aged males, which would be considered old in natural populations, gained most extra-pair paternity. However, both, female solicitation behaviour and subsequent extra-pair matings were not associated with male age. Further, copulations were more likely when solicited by females than when initiated by males (i.e. unsolicited copulations). Male initiated within-pair copulations were more common than male initiated extra-pair copulations. To conclude, our results did not support either hypothesis regarding age-specific male mating behaviour. Instead, female choice, independent of male age, governed copulation success, especially in an extra-pair context. Post-copulatory mechanisms might determine why older males sire more extra-pair offspring.
| S-EPMC5976671 | biostudies-literature
Project description:Since the first molecular study providing evidence for mating outside the pair bond in birds over 30 years ago, >500 studies have reported rates of extra-pair paternity (EPP) in >300 bird species. Here, we give a detailed overview of the current literature reporting EPP in birds and highlight the sampling biases and patterns in the data set with respect to taxonomy, avian phylogeny and global regions, knowledge of which will be crucial for correct interpretation of results in future comparative studies. Subsequently, we use this comprehensive dataset to simultaneously test the role of several ecological and life history variables. We do not find clear evidence that variation in EPP across socially monogamous species can be explained by latitude, density (coloniality), migration, generation length, genetic structuring (dispersal distance), or climatic variability, after accounting for phylogeny. These results contrast previous studies, most likely due to the large heterogeneity within species in both EPP and the predictor of interest, indicating that using species averages might be unreliable. Despite the absence of broadscale ecological drivers in explaining interspecific variation in EPP, we suggest that certain behaviours and ecological variables might facilitate or constrain EPP, as indicated by our finding that EPP was negatively associated with latitude within noncolonial species, suggesting a role of breeding synchrony. Thus, rather than focussing on general explanations for variation in EPP across all species, a future focus should be on how various aspects of ecology or life history might have driven variation in EPP among groups of species or populations of the same species. Hence, we argue that variation in EPP can be partly explained when taking the right perspective. This comprehensive overview, and particularly the dataset provided herein will create a foundation for further studies.
| S-EPMC6899757 | biostudies-literature
Project description:Females of many socially monogamous species accept or even actively seek copulations outside the social pair bond. As females cannot increase the number of offspring with promiscuous behaviour, the question arises why they engage in extra-pair mating. We used microsatellite data to determine paternity, heterozygosity and genetic relatedness in the reed bunting (Emberiza schoeniclus), a species with high levels of extra-pair paternity (EPP). We found that extra-pair young (EPY) were more heterozygous than within-pair young (WPY). The high heterozygosity of the EPY resulted from a low genetic similarity between females and their extra-pair mates. EPY were heavier and larger when compared with their maternal half-siblings shortly before they left the nest. Recapture data indicated a higher fledgling survival of EPY compared with WPY. Our data suggest that reed bunting females increase the viability of their offspring and thus fitness through extra-pair mating with genetically dissimilar males.
| S-EPMC2288684 | biostudies-literature